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Genome-wide survey and expression analysis of the bHLH-PAS genes in the amphioxus Branchiostoma floridae reveal both conserved and diverged expression patterns between cephalochordates and vertebrates.

Li KL, Lu TM, Yu JK - Evodevo (2014)

Bottom Line: The bHLH-PAS transcription factors are found in both protostomes and deuterostomes.These results imply that there were changes in gene regulation after the divergence of cephalochordates and vertebrates.In a comparison with the expression patterns of the vertebrate bHLH-PAS paralogs, which are the result of whole-genome duplication, we found that although several members seem to retain conserved expression patterns during chordate evolution, many duplicated paralogs may have undergone subfunctionalization and neofunctionalization in the vertebrate lineage.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Cellular and Organismic Biology, Academia Sinica, 128 Academia Road, Section 2, Nankang, Taipei 11529, Taiwan ; Institute of Oceanography, National Taiwan University, Taipei 10617, Taiwan.

ABSTRACT

Background: The bHLH-PAS transcription factors are found in both protostomes and deuterostomes. They are involved in many developmental and physiological processes, including regional differentiation of the central nervous system, tube-formation, hypoxia signaling, aromatic hydrocarbon sensing, and circadian rhythm regulation. To understand the evolution of these genes in chordates, we analyzed the bHLH-PAS genes of the basal chordate amphioxus (Branchiostoma floridae).

Results: From the amphioxus draft genome database, we identified ten bHLH-PAS genes, nine of which could be assigned to known orthologous families. The tenth bHLH-PAS gene could not be assigned confidently to any known bHLH family; however, phylogenetic analysis clustered this gene with arthropod Met family genes and two spiralian bHLH-PAS-containing sequences, suggesting that they may share the same ancestry. We examined temporal and spatial expression patterns of these bHLH-PAS genes in developing amphioxus embryos. We found that BfArnt, BfNcoa, BfSim, and BfHifα were expressed in the central nervous system in patterns similar to those of their vertebrate homologs, suggesting that their functions may be conserved. By contrast, the amphioxus BfAhr and BfNpas4 had expression patterns distinct from those in vertebrates. These results imply that there were changes in gene regulation after the divergence of cephalochordates and vertebrates.

Conclusions: We have identified ten bHLH-PAS genes from the amphioxus genome and determined the embryonic expression profiles for these genes. In addition to the nine currently recognized bHLH-PAS families, our survey suggests that the BfbHLHPAS-orphan gene along with arthropod Met genes and the newly identified spiralian bHLH-PAS-containing sequences represent an ancient group of genes that were lost in the vertebrate lineage. In a comparison with the expression patterns of the vertebrate bHLH-PAS paralogs, which are the result of whole-genome duplication, we found that although several members seem to retain conserved expression patterns during chordate evolution, many duplicated paralogs may have undergone subfunctionalization and neofunctionalization in the vertebrate lineage. In addition, our survey of amphioxus bHLH-PAS gene models from genome browser with experimentally verified cDNA sequences calls into question the accuracy of the current in silico gene annotation of the B. floridae genome.

No MeSH data available.


Related in: MedlinePlus

Expression of BfNcoa.In situ hybridization of BfNcoa with antisense probe and with sense probe. (A-F) Ubiquitous expression is shown from blastula to early neurula. (G-N) From mid-neurula, tissue-specific signal is detected in some paired cell groups in the anterior central nervous system (arrowheads). (O,P) At the larval stage, stronger expression is observed in the cerebral vesicle (arrow), and weaker expression is observed in the neural tube. (Q,R) No apparent expression is found in the gut. The scale bar in panel A applies to panels A-P. Blastoporal views (bp) and dorsal views (d) are labeled, and unlabeled panels are lateral views. In E-J, anterior is to the left; in K-R, anterior is to the upper left. Boundaries of somites are depicted in I.
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Figure 5: Expression of BfNcoa.In situ hybridization of BfNcoa with antisense probe and with sense probe. (A-F) Ubiquitous expression is shown from blastula to early neurula. (G-N) From mid-neurula, tissue-specific signal is detected in some paired cell groups in the anterior central nervous system (arrowheads). (O,P) At the larval stage, stronger expression is observed in the cerebral vesicle (arrow), and weaker expression is observed in the neural tube. (Q,R) No apparent expression is found in the gut. The scale bar in panel A applies to panels A-P. Blastoporal views (bp) and dorsal views (d) are labeled, and unlabeled panels are lateral views. In E-J, anterior is to the left; in K-R, anterior is to the upper left. Boundaries of somites are depicted in I.

Mentions: Figure 5 shows the expression of BfNcoa. Before the blastula stage, the BfNcoa transcripts were distributed ubiquitously (Figure 5A). From N2 stage, tissue-specific expression was detected in some cells inside the CNS (arrowheads, Figure 5G,I). These paired cells were located in the neural tube from the second to fourth somite level, just posterior to the cerebral vesicle. At the early larval stage (L1), strong expression was detected in two rows of cells inside the neural tube (Figure 5K,M); subsequently in the late larval stage (L3), only weak expression was detected in the anterior neural tube (Figure 5O).


Genome-wide survey and expression analysis of the bHLH-PAS genes in the amphioxus Branchiostoma floridae reveal both conserved and diverged expression patterns between cephalochordates and vertebrates.

Li KL, Lu TM, Yu JK - Evodevo (2014)

Expression of BfNcoa.In situ hybridization of BfNcoa with antisense probe and with sense probe. (A-F) Ubiquitous expression is shown from blastula to early neurula. (G-N) From mid-neurula, tissue-specific signal is detected in some paired cell groups in the anterior central nervous system (arrowheads). (O,P) At the larval stage, stronger expression is observed in the cerebral vesicle (arrow), and weaker expression is observed in the neural tube. (Q,R) No apparent expression is found in the gut. The scale bar in panel A applies to panels A-P. Blastoporal views (bp) and dorsal views (d) are labeled, and unlabeled panels are lateral views. In E-J, anterior is to the left; in K-R, anterior is to the upper left. Boundaries of somites are depicted in I.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4066832&req=5

Figure 5: Expression of BfNcoa.In situ hybridization of BfNcoa with antisense probe and with sense probe. (A-F) Ubiquitous expression is shown from blastula to early neurula. (G-N) From mid-neurula, tissue-specific signal is detected in some paired cell groups in the anterior central nervous system (arrowheads). (O,P) At the larval stage, stronger expression is observed in the cerebral vesicle (arrow), and weaker expression is observed in the neural tube. (Q,R) No apparent expression is found in the gut. The scale bar in panel A applies to panels A-P. Blastoporal views (bp) and dorsal views (d) are labeled, and unlabeled panels are lateral views. In E-J, anterior is to the left; in K-R, anterior is to the upper left. Boundaries of somites are depicted in I.
Mentions: Figure 5 shows the expression of BfNcoa. Before the blastula stage, the BfNcoa transcripts were distributed ubiquitously (Figure 5A). From N2 stage, tissue-specific expression was detected in some cells inside the CNS (arrowheads, Figure 5G,I). These paired cells were located in the neural tube from the second to fourth somite level, just posterior to the cerebral vesicle. At the early larval stage (L1), strong expression was detected in two rows of cells inside the neural tube (Figure 5K,M); subsequently in the late larval stage (L3), only weak expression was detected in the anterior neural tube (Figure 5O).

Bottom Line: The bHLH-PAS transcription factors are found in both protostomes and deuterostomes.These results imply that there were changes in gene regulation after the divergence of cephalochordates and vertebrates.In a comparison with the expression patterns of the vertebrate bHLH-PAS paralogs, which are the result of whole-genome duplication, we found that although several members seem to retain conserved expression patterns during chordate evolution, many duplicated paralogs may have undergone subfunctionalization and neofunctionalization in the vertebrate lineage.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Cellular and Organismic Biology, Academia Sinica, 128 Academia Road, Section 2, Nankang, Taipei 11529, Taiwan ; Institute of Oceanography, National Taiwan University, Taipei 10617, Taiwan.

ABSTRACT

Background: The bHLH-PAS transcription factors are found in both protostomes and deuterostomes. They are involved in many developmental and physiological processes, including regional differentiation of the central nervous system, tube-formation, hypoxia signaling, aromatic hydrocarbon sensing, and circadian rhythm regulation. To understand the evolution of these genes in chordates, we analyzed the bHLH-PAS genes of the basal chordate amphioxus (Branchiostoma floridae).

Results: From the amphioxus draft genome database, we identified ten bHLH-PAS genes, nine of which could be assigned to known orthologous families. The tenth bHLH-PAS gene could not be assigned confidently to any known bHLH family; however, phylogenetic analysis clustered this gene with arthropod Met family genes and two spiralian bHLH-PAS-containing sequences, suggesting that they may share the same ancestry. We examined temporal and spatial expression patterns of these bHLH-PAS genes in developing amphioxus embryos. We found that BfArnt, BfNcoa, BfSim, and BfHifα were expressed in the central nervous system in patterns similar to those of their vertebrate homologs, suggesting that their functions may be conserved. By contrast, the amphioxus BfAhr and BfNpas4 had expression patterns distinct from those in vertebrates. These results imply that there were changes in gene regulation after the divergence of cephalochordates and vertebrates.

Conclusions: We have identified ten bHLH-PAS genes from the amphioxus genome and determined the embryonic expression profiles for these genes. In addition to the nine currently recognized bHLH-PAS families, our survey suggests that the BfbHLHPAS-orphan gene along with arthropod Met genes and the newly identified spiralian bHLH-PAS-containing sequences represent an ancient group of genes that were lost in the vertebrate lineage. In a comparison with the expression patterns of the vertebrate bHLH-PAS paralogs, which are the result of whole-genome duplication, we found that although several members seem to retain conserved expression patterns during chordate evolution, many duplicated paralogs may have undergone subfunctionalization and neofunctionalization in the vertebrate lineage. In addition, our survey of amphioxus bHLH-PAS gene models from genome browser with experimentally verified cDNA sequences calls into question the accuracy of the current in silico gene annotation of the B. floridae genome.

No MeSH data available.


Related in: MedlinePlus